食蟹猴源弗氏柠檬酸杆菌的分离鉴定及生物学特性分析

doi:10.12300/j.issn.1674-5817.2025.150

实验动物与比较医学 ›› 2026, Vol. 46 ›› Issue (3): 367-377.DOI: 10.12300/j.issn.1674-5817.2025.150

食蟹猴源弗氏柠檬酸杆菌的分离鉴定及生物学特性分析

李鹤龄¹, 钱子瑶¹, 覃刚民², 蒋德兵², 张艳琼², 金文政², 王宏¹^,²()()

^1.昆明理工大学灵长类转化医学研究院, 昆明 650500
^2.云南中科灵长类生物医学重点实验室, 昆明 650500

收稿日期:2025-09-16 修回日期:2025-12-02 出版日期:2026-06-25 发布日期:2026-06-19
通讯作者:
王宏（1975—），男，博士，研究员，研究方向：实验动物疾病的诊断与治疗。E-mail：wangh@lpbr.cn。ORCID：0009-0004-6763-3168
作者简介:李鹤龄（1990—），女，硕士，高级兽医师，研究方向：非人灵长类动物疾病的诊断与治疗。E-mail：lihl@lpbr.cn
基金资助:
云南省自然科学基金项目“灵长类生殖发育与人类重大疾病的机制及转化研究”(202001BC070001)

Isolation, Identification and Biological Characteristics Analysis of Citrobacter freundii from Cynomolgus Monkey (Macaca fascicularis)

LI Heling¹, QIAN Ziyao¹, QIN Gangmin², JIANG Debing², ZHANG Yanqiong², JIN Wenzheng², WANG Hong¹^,²()()

^1.Institute of Primate Translational Medicine, Kunming University of Science and Technology, Kunming 650500, China
^2.Yunnan Key Laboratory of Primate Biomedical Research, Kunming 650500, China

Received:2025-09-16 Revised:2025-12-02 Published:2026-06-25 Online:2026-06-19
Correspondence to: WANG Hong (ORCID: 0009-0004-6763-3168), E-mail: wangh@lpbr.cn

摘要/Abstract

摘要：

目的对1株导致食蟹猴腹泻的致病菌进行鉴定分析、动物回归试验和药物敏感性研究，为弗氏柠檬酸杆菌的临床治疗提供实践依据。方法收集9只腹泻食蟹猴的新鲜粪便，分别划线接种于沙门-志贺氏（Salmonella-Shigella，SS）培养基、LB培养基和哥伦比亚血琼脂培养基，37 ℃恒温培养24 h。随后通过菌落形态观察、革兰氏染色、生化试验和16S rRNA基因测序对分离菌株进行鉴定，并采用PCR方法检测分离菌株的主要毒力基因；将分离菌增殖后灌胃健康食蟹猴和C57BL/6小鼠进行动物回归试验，以分析菌株的致病性；最后，采用圆片扩散法检测分离菌株的药物敏感性。结果从9只腹泻食蟹猴的粪便样本中共分离到1株细菌，命名为MF071743。该分离菌株在SS培养基上形成粉红色、光滑的圆形菌落；在LB培养基上形成光滑、湿润、表面有光泽、边缘整齐的半透明菌落；在哥伦比亚血琼脂上形成光滑湿润的灰白色菌落。革兰氏染色结果显示，该菌株为革兰氏阴性、无芽孢短杆菌。生化实验结果显示，该分离菌株动力试验为阳性，甘露醇试验、硫化氢试验、甲基红试验、枸橼酸盐利用试验、葡萄糖产气试验、棉子糖试验、山梨醇试验和D-木糖发酵试验均为阳性，但苯丙氨酸试验、葡萄糖酸盐试验、吲哚试验、伏-波（Voges Proskauer，VP）试验、脲酶试验、赖氨酸试验、鸟氨酸试验和侧金盏花醇试验均为阴性。16S rRNA基因测序结果显示，MF071743与弗氏柠檬酸杆菌基因组的相似度高达99.0%。PCR结果显示，该菌株携带编码脲酶辅助蛋白（urease accessory protein，ure）D、ureE和ureF的基因。动物灌胃实验结果显示，该菌株能导致食蟹猴粪便稀软，C57BL/6小鼠72 h内全部死亡（100%）。药敏试验结果显示，该菌株对头孢曲松、阿米卡星、庆大霉素、头孢他啶、左氧氟沙星等16种药物敏感，对氨苄西林、头孢唑林、万古霉素、红霉素和头孢氨苄耐药。结论从食蟹猴腹泻粪便中分离到1株弗氏柠檬酸杆菌，该菌株对多种抗生素具有耐药性，本研究结果为圈养实验猴消化道疾病的诊断和治疗提供了参考。

关键词: 食蟹猴, 弗氏柠檬酸杆菌, 细菌培养, 分离鉴定, 系统发育分析

Abstract:

Objective Identification and analysis, animal regression test, and drug susceptibility study were conducted on a pathogenic strain causing diarrhea in cynomolgus monkeys, aiming to provide a practical basis for the clinical treatment of Citrobacter freundii. Methods Fresh fecal samples were collected from nine diarrheal cynomolgus monkeys and streaked on Salmonella-Shigella (SS) medium, LB medium, and Columbia blood agar medium, and incubated at 37 ℃ for 24 h. Subsequently, the isolated strain was identified by colony morphology observation, Gram staining, biochemical tests and 16S rRNA gene sequencing, and PCR was used to detect its major virulence genes. After propagation, the isolate was intragastrically administered to healthy cynomolgus monkeys and C57BL/6 mice for animal regression tests to evaluate its pathogenicity. Finally, the disk-diffusion method was used to detect the antimicrobial susceptibility of the isolate. Results A single bacterial strain, designated MF071743, was isolated from 9 fecal samples collected from diarrheal cynomolgus monkeys. The isolate formed pink, smooth, round colonies on SS medium; translucent, smooth, moist, shiny colonies with neat edges on LB medium; and smooth, moist, off-white colonies on Columbia blood agar medium. Gram staining revealed that the isolate was a Gram-negative, spore-free short bacillus. Biochemical tests showed that the isolate was positive for motility test, mannitol test, hydrogen sulfide test, methyl red test, citrate utilization test, gas production from glucose test, raffinose test, sorbitol test, and D-xylose test, but negative for phenylalanine test, gluconate test, indole test, Voges Proskauer (VP) test, urease test, lysine test, ornithine test, and adonitol test. The results of 16S rRNA gene sequencing showed that the gene sequence similarity between strain MF071743 and Citrobacter freundii was 99.0%. PCR results showed that this strain carries genes encoding the urease accessory proteins UreD, UreE, and UreF. Animal intragastric administration assays demonstrated that the strain caused loose stools in cynomolgus monkeys, and all C57BL/6 mice died within 72 h. Drug susceptibility test results indicated that the isolate was sensitive to 16 antibiotics, including ceftriaxone, amikacin, gentamicin, ceftazidime, and levofloxacin, while it exhibited resistance to 5 antibiotics, including ampicillin, cefazolin, vancomycin, erythromycin, and cephalexin. Conclusion A strain of Citrobacter freundii with certain drug resistance was isolated from the feces of diarrheal cynomolgus monkeys. The results of this study provide a reference for the diagnosis and treatment of gastrointestinal diseases in captive laboratory monkeys.

Key words: Cynomolgus monkey, Citrobacter freundii, Bacterial culture, Isolation and identification, Phylogenetic analysis

中图分类号:

S852.61
S858

李鹤龄,钱子瑶,覃刚民,等. 食蟹猴源弗氏柠檬酸杆菌的分离鉴定及生物学特性分析[J]. 实验动物与比较医学, 2026, 46(3): 367-377. DOI: 10.12300/j.issn.1674-5817.2025.150.

LI Heling,QIAN Ziyao,QIN Gangmin,et al. Isolation, Identification and Biological Characteristics Analysis of Citrobacter freundii from Cynomolgus Monkey (Macaca fascicularis)[J]. Laboratory Animal and Comparative Medicine, 2026, 46(3): 367-377. DOI: 10.12300/j.issn.1674-5817.2025.150.

图/表 7

表1 细菌16S rRNA引物和弗氏柠檬酸杆菌主要毒力基因引物
注：cfa，定居因子抗原；ure，脲酶辅助蛋白；F，正向引物；R，反向引物。

Table 1 Primer sequences of 16S rRNA and major virulence genes of Citrobacter freundii
Note：cfa， colonization factor antigen；ure， urease accessory protein； F， forward primer； R， reverse primer

引物名称 Primer name	引物序列(5'→3') Primer sequence (5'→3')		退火温度/℃ Annealing temperature/℃	预期长度/bp Expected length/bp
16S rRNA	F: AGAGTTTGATCCTGGCTCAG	R: CGGTTACCTTGTTACGACTT	55.0	1 500
cfa	F: TCCAGCGCATTCA	R: TCCAGCCTTCGGCAAACG	60.5	100
ureABC	F: ATGGAACTGACTCCCAGAG	R: TCAAAACAGAAAATAGCGTTGCGCC	56.5	2 328
ureD	F: CCGCAAGAGGACGTTTGC	R: CCGACCCAGGGATGATGT	60.0	459
ureE	F: ACCCAACGCCTTGACCAC	R: AGGATTTGCAGCGGAACG	63.7	293
ureF	F: TGGAAATCGGCTGGGTGA	R: CCCGACTGCGTTCTTCATC	65.0	210
ureG	F: ATCAGCGCATTCTCACCG	R: CAATAATCGTCGCCAGACC	53.2	438

图1 食蟹猴肛拭子样本分离菌株的形态特征
注：A～C，分别为分离菌株在沙门-志贺氏（SS）、LB和哥伦比亚血琼脂培养基上的生长情况；D，分离菌株的革兰氏染色结果。比例尺为10 μm。

Figure 1 Morphological characteristics of the isolated strain from cynomolgus monkey anal swab samples
Note： A-C， Growth morphology of the isolated strain on the Salmonella-Shigella （SS）， LB， and Columbia blood agar media； D， Gram staining result of the isolated strain. Scale bar = 10 μm.

表2 分离菌株MF071743的生化检测结果
注：+表示阳性；－表示阴性；±表示不定型。

Table 2 Biochemical test results of the isolated strain MF071743
Note： + indicates positive；－ indicates negative； ± indicates indeterminate type．

检测项目 Test items	结果 Results	标准菌株 Reference strains
甘露醇试验 Mannitol test	+	+
硫化氢试验 H₂S test	+	±
苯丙氨酸试验 Phenylalanine test	-	-
葡萄糖酸盐试验 Gluconate test	-	-
吲哚试验 Indigo test	-	±
VP试验 Voges Proskauer test	-	-
甲基红试验 Methyl red test	+	+
枸橼酸盐试验 Citrate test	+	±
脲酶试验 Urease test	-	±
葡萄糖产气试验 Glucose gas production test	+	±
赖氨酸试验 Lysine test	-	-
鸟氨酸试验 Ornithine test	-	±
棉子糖试验 Raffinose test	+	±
山梨醇试验 Sorbitol test	+	±
侧金盏花醇试验 Adonitol test	-	-
木糖试验 Xylose test	+	±

图2 食蟹猴粪便分离菌株16S rRNA基因的PCR扩增结果
注：M，DNA marker；1，样品；N，阴性对照。

Figure 2 PCR amplification of the 16S rRNA gene of the strain isolated from cynomolgus monkey feces
Note： M， DNA marker； 1， sample； N， negative control.

图3 分离菌株MF071743与不同来源弗氏柠檬酸杆菌的同源性比对（A）及基于16S rRNA序列的系统进化树（B）
注：▲本试验食蟹猴源分离菌株。

Figure 3 Homology comparison between the isolated strain MF071743 and Citrobacter freundii from different sources （A） and a phylogenetic tree based on 16S rRNA sequences（B）
Note： ▲ Isolated strain from cynomolgus monkey in this study.

图4 弗氏柠檬酸杆菌主要毒力基因的PCR扩增结果
注：M，DNA marker；1，阴性对照；2，定居因子抗原（cfa）；3，脲酶结构基因ABC（ureABC）；4，脲酶辅助基因D（ureD）；5，脲酶辅助基因E（ureE）；6，脲酶辅助基因F（ureF）；7，脲酶辅助基因G（ureG）。

Figure 4 PCR amplification results of major virulence genes of Citrobacter freundii
Note： M， DNA marker； 1，negative control；2，colonization factor antigen； 3，urease structural gene ABC； 4，urease accessory gene D； 5，urease accessory gene E； 6， urease accessory gene F； 7， urease accessory gene G.

表3 弗氏柠檬酸杆菌分离株的药敏试验结果
注：R，耐药；I，中介；S，敏感。各药物含量数据来自药品使用说明书。

Table 3 Drug susceptibility test results of the isolated strain of Citrobacter freundii
Note：R， resistant； I， intermediate； S， sensitivity. Data of each drug's content were derived from pharmaceutical specifications

药物 Drug	药物含量/（µg·片^-1) Drug dose /(µg·disc^-1)	抑菌圈直径/mm Inhibition zone diameter/mm	判定结果 Assessment result	判定标准/mm Judgement standard/mm
药物 Drug	药物含量/（µg·片^-1) Drug dose /(µg·disc^-1)	抑菌圈直径/mm Inhibition zone diameter/mm	判定结果 Assessment result	R	I	S
头孢曲松 Ceftriaxone	30	30	S	≤13	14～22	≥23
阿米卡星 Amikacin	30	24	S	≤14	15～16	≥17
庆大霉素 Gentamicin	10±2.5	19	S	≤12	13～14	≥15
氨苄西林 Ampicillin	10	10	R	≤13	14～16	≥17
头孢唑啉 Cefazolin	30	7	R	≤14	15～17	≥18
头孢他啶 Ceftazidime	30	26	S	≤17	18～20	≥21
左氧氟沙星 Levofloxacin	5	28	S	≤13	14～16	≥17
万古霉素 Vancomycin	30	7	R	≤9	10～11	≥12
复方磺胺甲��唑 Co-trimoxazole	23.75	24	S	≤10	11～15	≥16
环丙沙星 Ciprofloxacin	5	29	S	≤15	16～20	≥21
诺氟沙星 Norfloxacin	10	27	S	≤12	13～16	≥17
红霉素 Erythromycin	15	7	R	≤13	14～22	≥23
利福平 Rifampicin	5	7	I	≤6	7～9	≥10
阿莫西林 Amoxicillin	10	10	S	≤5	6～9	≥10
呋喃唑酮 Furazolidone	300	18	S	≤5	6～9	≥10
林可霉素 Lincomycin	2	7	I	≤5	6～11	≥12
多黏菌素B Polymyxin B	300	13	S	≤8	9～11	≥12
头孢哌酮 Cefoperazone	75	31	S	≤15	16～20	≥21
头孢氨苄 Cephalexin	30	7	R	≤13	14～16	≥17
氧氟沙星 Ofloxacin	5	28	S	≤12	13～15	≥16
杆菌肽 Bacitracin	0.04	7	I	≤6	7～9	≥10
亚胺培南 Imipenem	10	23	S	≤19	20～22	≥23
美罗培南 Meropenem	10	28	S	≤19	20～22	≥23
阿奇霉素 Azithromycin	15	18	S	≤12	–	≥13

表3 弗氏柠檬酸杆菌分离株的药敏试验结果
注：R，耐药；I，中介；S，敏感。各药物含量数据来自药品使用说明书。

药物 Drug	药物含量/（µg·片^-1) Drug dose /(µg·disc^-1)	抑菌圈直径/mm Inhibition zone diameter/mm	判定结果 Assessment result	判定标准/mm Judgement standard/mm
药物 Drug	药物含量/（µg·片^-1) Drug dose /(µg·disc^-1)	抑菌圈直径/mm Inhibition zone diameter/mm	判定结果 Assessment result	R	I	S
头孢曲松 Ceftriaxone	30	30	S	≤13	14～22	≥23
阿米卡星 Amikacin	30	24	S	≤14	15～16	≥17
庆大霉素 Gentamicin	10±2.5	19	S	≤12	13～14	≥15
氨苄西林 Ampicillin	10	10	R	≤13	14～16	≥17
头孢唑啉 Cefazolin	30	7	R	≤14	15～17	≥18
头孢他啶 Ceftazidime	30	26	S	≤17	18～20	≥21
左氧氟沙星 Levofloxacin	5	28	S	≤13	14～16	≥17
万古霉素 Vancomycin	30	7	R	≤9	10～11	≥12
复方磺胺甲��唑 Co-trimoxazole	23.75	24	S	≤10	11～15	≥16
环丙沙星 Ciprofloxacin	5	29	S	≤15	16～20	≥21
诺氟沙星 Norfloxacin	10	27	S	≤12	13～16	≥17
红霉素 Erythromycin	15	7	R	≤13	14～22	≥23
利福平 Rifampicin	5	7	I	≤6	7～9	≥10
阿莫西林 Amoxicillin	10	10	S	≤5	6～9	≥10
呋喃唑酮 Furazolidone	300	18	S	≤5	6～9	≥10
林可霉素 Lincomycin	2	7	I	≤5	6～11	≥12
多黏菌素B Polymyxin B	300	13	S	≤8	9～11	≥12
头孢哌酮 Cefoperazone	75	31	S	≤15	16～20	≥21
头孢氨苄 Cephalexin	30	7	R	≤13	14～16	≥17
氧氟沙星 Ofloxacin	5	28	S	≤12	13～15	≥16
杆菌肽 Bacitracin	0.04	7	I	≤6	7～9	≥10
亚胺培南 Imipenem	10	23	S	≤19	20～22	≥23
美罗培南 Meropenem	10	28	S	≤19	20～22	≥23
阿奇霉素 Azithromycin	15	18	S	≤12	–	≥13

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食蟹猴源弗氏柠檬酸杆菌的分离鉴定及生物学特性分析

Isolation, Identification and Biological Characteristics Analysis of Citrobacter freundii from Cynomolgus Monkey (Macaca fascicularis)

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